Clinical Applications of Transthoracic Ultrasound in Chest Medicine

Clinical Applications of Transthoracic Ultrasound in Chest Medicine

R E V I E W A R T I C L E Clinical Applications of Transthoracic Ultrasound in Chest Medicine Tzu-Hsiu Tsai, Jih-Shuin Jerng*, Pan-Chyr Yang Transtho...

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Clinical Applications of Transthoracic Ultrasound in Chest Medicine Tzu-Hsiu Tsai, Jih-Shuin Jerng*, Pan-Chyr Yang Transthoracic ultrasound (US) has become an important diagnostic tool in modern chest medicine. The range of thoracic lesions for which transthoracic US may yield useful diagnostic information has expanded to include not only chest wall and pleural lesions, but also peripheral lung nodules, pulmonary consolidations, necrotizing pneumonias and lung abscesses, tumors with obstructive pneumonitis, mediastinal masses, and peridiaphragmatic lesions. A variety of ultrasound features and signs of chest diseases have been well characterized and widely applied in clinical practice. US guidance increases the diagnostic success rate and decreases the complications associated with interventional procedures such as thoracentesis, closed tube drainage for pleural effusion, and needle biopsy of the pleura. Transthoracic needle aspiration or biopsy, under real-time US guidance, is a relatively safe and easy procedure, and may provide adequate tissue sampling of lesions for cytologic, histologic or microbiologic analysis. This article presents the general techniques and wide applications of transthoracic US and US-guided invasive procedures in the diagnosis and management of various chest diseases.

KEY WORDS — chest diseases, transthoracic needle biopsy, transthoracic ultrasound ■ J Med Ultrasound 2008;16(1):7–25 ■

Introduction Advances in technology in recent decades have greatly improved the imaging capacity of ultrasound (US). Major advantages of US include the absence of radiation, low cost, flexibility, bedside availability, and short examination time compared with computed tomography [1]. US is notably helpful for critically ill patients because of its portability and simplicity [2]. By scanning through the acoustic window, transthoracic US has proved to be a reliable and informative imaging tool for the evaluation of

a wide variety of complex chest diseases. Many US features and signs of chest diseases have been well characterized and widely applied in clinical practice. Transthoracic US can supplement other imaging modalities of the chest and guide a variety of diagnostic and therapeutic procedures. Under realtime US guidance, the success rate of transthoracic needle aspiration or biopsy (TNB) significantly increases, whereas the risk of complications is greatly reduced [1,3–7]. This article presents an overview of the wide applications of transthoracic US and US-guided interventional procedures in

Received: September 5, 2007 Accepted: January 22, 2008 Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan. *Address correspondence to: Dr. Jih-Shuin Jerng, Department of Internal Medicine, National Taiwan University Hospital, 7 Chung-Shan South Road, Taipei 100, Taiwan. E-mail: [email protected]

©Elsevier & CTSUM. All rights reserved.

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T.H. Tsai, J.S. Jerng, P.C. Yang the diagnosis and management of various chest diseases with clinical examples, and describes patient selection and indications, general imaging techniques, US images of normal chest, ultrasonographic characteristics of various chest diseases, and US-guided interventional procedures.

Techniques for Transthoracic US Examination and Normal US Images of the Chest Patient selection and indications Evaluation of thoracic lesions using transthoracic US is inherently hindered for two reasons. Firstly, the lungs are well concealed by the bony ribs, scapulae, and spine. Secondly, the air-containing lung parenchyma is a poor US transmitter and reflects most of the US beam. Structures located deep within a normally aerated lung are not visualized with transthoracic US. Therefore, the application of transthoracic US is restricted to those with an available “US window”, which allows the US beam to penetrate, allowing visualization of the target lesion [1,3,4]. The US window used most often is chest wall, atelectatic or consolidated lung, or pleural fluid interposed between the lesion and chest wall (Fig. 1). The following lesions are thus suited to

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transthoracic US examination: (1) chest wall lesions; (2) pleural lesions such as pleural effusion, pleural thickening or pleural tumors; (3) peridiaphragmatic lesions; (4) peripheral pulmonary lesions which abut the pleura; (5) pulmonary lesions with an accessible US window; and (6) mediastinal tumors in contact with the chest wall [1,3,4,7]. In general, indications for US-guided interventional procedures include: (1) identifying pleural effusion and guiding thoracentesis and drainage for effusion, especially when the effusion is minimal or loculated; (2) localizing pleural thickening or tumors for pleural biopsy; (3) identifying peripheral pulmonary nodules and guiding TNB to determine etiology of the lesion, particularly when cancer or infection is suspected; (4) evaluating the nature of pulmonary consolidation of unknown etiology; (5) needle aspiration of the cavity of a necrotizing pneumonia or lung abscess for microbiologic diagnosis; (6) identifying the central tumor producing obstructive pneumonitis and guiding TNB of the tumor for histologic diagnosis, especially when fiberoptic bronchoscopy is not feasible; (7) evaluating a mediastinal tumor and guiding TNB for histologic diagnosis; (8) identifying the nature of a chest wall lesion and guiding needle sampling; and (9) assisting in the assessment of cervical lymphadenopathy in patients with lung cancer [1,3–7].

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Fig. 1. Pleural effusion as an ultrasound (US) window for approach of a lung tumor. (A) Computed tomography scan shows a lung tumor and right pleural effusion in an 81-year-old man. (B) The pleural effusion interposed between the tumor and chest wall creates a US window, allowing visualization of the lung tumor with transthoracic US. The histologic diagnosis of lung cancer was obtained by transthoracic needle biopsy under US guidance. E = effusion; T = tumor.

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Transthoracic Ultrasound

General techniques for transthoracic US examination The equipment suitable for transthoracic US imaging are those equipped with 3.5-, 5-, 7.5-, or 10-MHz convex, linear and sector transducers. Most series also provide both color Doppler US and amplitude US angiography software which can be used to detect blood flow signals. A higher frequency (i.e. 7.5- or 10-MHz) transducer provides better resolution of near structures, such as the chest wall and pleura. Otherwise, a 3.5-MHz transducer is more suitable for visualization of deeper lesions. A linear or convex transducer usually has a broad view of the field and is better than a sector scanner for screening. For lesions with a small US window or a very narrow intercostal space, a sector transducer is generally preferred [1,3,7]. During transthoracic US examination, the patient can be scanned in the sitting or supine position. Bedridden patients can be examined in the lateral decubitis or oblique position. After applying US transmission gel, the probe is moved in transverse or longitudinal directions along the intercostal spaces to avoid interference by the bony ribs. The lesion is first localized using grayscale, real-time US imaging, and normal areas are also scanned for control comparisons. The location, sonographic appearance and echogenicity, and vascularity of the lesion are characterized, with the latter characteristic determined by color Doppler US [8]. The liver and fasted gallbladder can be used as tissuetexture references for solid and fluid-containing regions. Hence, the echogenicity of a lesion is compared with that of the liver and defined as hypoechoic, isoechoic or hyperechoic accordingly.

are seen as two thin and bright echogenic lines. Normally, the two pleural lines are smooth and less than 2 mm in thickness [9]. Because of the movements of the pleurae during lung excursion, the two pleural lines glide with each other during respiration on real-time US. This is termed “lung sliding” or “gliding sign” of the pleurae [10]. Small uneven irregularities of the visceral pleura may produce vertical reverberations known as “comettail artifacts” [9,11] (Fig. 2). However, with a 3.5MHz transducer, it is not always possible to visualize the two pleural lines and the pleural space between them. Instead, a highly echogenic line representing the pleurae and the pleuropulmonary surface is seen with reverberation echo artifacts just beneath it. Back-and-forth movements of this echogenic pleural line during respiration can still be observed on real-time US. The underlying air-filled lung is a highly reflective interface that may block transmission of US into the lung parenchyma. US images of the lung parenchyma thus display a pattern of repeated horizontal echoes caused by an acoustic reverberation artifact [11] (Fig. 2). These echoes may be bright but formless, and diminish rapidly in intensity with increasing distance from the transducer. Both hemidiaphragms can be visualized just above the liver and spleen, and the respiratory movements of both hemidiaphragms can be observed on real-time US. During inspiration, the reverberation echoes of the lower lung descend progressively with lung excursion and appear like a curtain. By defining the position of the hemidiaphragm, differentiation can be made between the thoracic and abdominal compartments.

Normal US images of the chest US images of the chest wall usually show soft tissue echogenicity with multiple layers of muscle and fascia. When the transducer is oriented perpendicular to the intercostal spaces, normal ribs may appear as curvilinear echogenic interfaces with prominent acoustic shadows. Just beneath the chest wall, the parietal pleura lining the bony thorax and the visceral pleura covering the lung

Diagnostic Scanning and Ultrasonographic Characteristics of Various Chest Diseases Chest wall lesions Chest wall lesions are superficial and typically suited for transthoracic US examination. These include lesions which are isolated to the chest wall J Med Ultrasound 2008 • Vol 16 • No 1

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Fig. 2. Normal ultrasound images of the chest. (A) Transverse image through the intercostal space using a 10-MHz scanner. The chest wall is visualized as multiple layers of echogenicity representing muscles and fasciae. The visceral and parietal pleurae appear as echogenic bright lines that glide during respiration (gliding sign). Reverberation echo artifacts beneath the pleural lines imply an underlying air-filled lung. (B) Longitudinal image across the ribs. Normal ribs are seen as hyperechoic chambered surfaces (arrowheads) with prominent acoustic shadows beneath the ribs. (C) Ultrasound image displaying comet-tail artifacts (arrows). Pp = parietal pleura; Pv = visceral pleura. and intrathoracic lesions that extend peripherally into the chest wall. On US, chest wall tumors usually appear as well-defined, hypoechoic masses within the soft tissue layers of the chest wall. Inflammatory lesions may show an irregular margin and heterogeneous internal echo texture. When the chest wall lesion invades the ribs, areas of destructive bone may be seen as eccentric, hyperechoic plate-like shadows inside the lesion. Osteolytic bone lesions caused by metastatic tumors generally appear as round or ring shadows within the center of a hypoechoic tumor (Fig. 3). USguided percutaneous aspiration or biopsy of chest wall lesions has been reported to have a very high diagnostic yield [12]. US is also useful for the evaluation of cervical and supraclavicular lymph nodes in patients with malignancy. Lymph nodes on US appear as round or ovoid, discrete hypoechoic nodules, or multiple confluent and lobulated masses within the soft tissue layers. Color Doppler US can be employed to differentiate the cross section of a vessel from a lymph node by detecting blood flow signals in the

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vessel [13]. In patients with palpable cervical lesions of unknown nature, US can differentiate lymph nodes from ligaments, thrombosed veins, scar tissue, nodular goiter, or fat pads. The cytologic features of affected lymph nodes can be clarified with the aid of aspiration cytology [14].

Pleural effusion US is very helpful in determining the nature of pleural lesions and is extremely sensitive in detecting pleural effusion. On US, pleural effusion is characterized by an echo-free or hypoechoic space between the visceral and parietal pleurae that can change shape with respiration (Fig. 4A). The effusion can be free or encapsulated. Compressive atelectasis of the lung in a large effusion may be seen as a tongue-like structure within the effusion. According to the internal echogenicity, effusion can be classified as anechoic, complex nonseptated, complex septated, and homogeneously echogenic [15]. The effusion is defined as anechoic if a totally echo-free space is present between the visceral and parietal pleurae, complex nonseptated

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Fig. 3. A 68-year-old man with metastatic lung cancer to the chest wall. (A) Computed tomography scan shows a soft tissue tumor with rib destruction (arrowheads). (B) Ultrasound reveals a well-defined, hypoechoic mass within the chest wall. The hyperechoic rings inside the hypoechoic tumor represent osteolytic ribs (arrows). T = tumor.

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Fig. 4. (A) Ultrasound image of minimal subpulmonary effusion seen as an echo-free space between the visceral pleura, parietal pleura, and diaphragm. This echo-free space may change shape with respiration. (B–E) The effusion can be subclassified as (B) anechoic, (C) complex nonseptated, (D) complex septated, and (E) homogenously echogenic. Note the movable echogenic densities within the complex nonseptated effusion, and the floating strands and septa within the complex septated effusion (arrows). D = diaphragm; L = collapsed lung; PE = pleural effusion. if echogenic materials are present inside the effusion, complex septated if floating strands or septa are present inside the effusion, and homogeneously echogenic if a homogeneously echogenic pleural

space is demonstrated (Figs. 4B–4E). The echogenic densities within a complex effusion probably reflect the presence of tissue debris, protein-rich particles, fibrins, or blood in the pleural fluid. Sonographic J Med Ultrasound 2008 • Vol 16 • No 1

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T.H. Tsai, J.S. Jerng, P.C. Yang characteristics of effusion are informative for differentiating transudate from exudate. In a study of 320 patients, it was found that a transudate was invariably anechoic, whereas an anechoic effusion can be either a transudate or an exudate. Pleural effusions with complex nonseptated, complex septated and homogeneously echogenic patterns are always exudative. Homogeneously echogenic effusion is typically seen in hemorrhagic effusion and empyema [15]. Other associated sonographic findings sometimes help to assess the nature of pleural effusion [7]. For example, effusion with adjacent thickened pleura is usually indicative of an exudate. The presence of a pulmonary consolidation may suggest an exudate of infectious origin. Pleural nodules may be seen in patients with malignant effusion [16]. In cases of acute thoracic empyema, it was reported that sonographic septation is a useful sign in predicting the need for subsequent intrapleural fibrinolytic therapy or surgical intervention [17]. Methods for measuring the volume of pleural effusion by means of US have been reported in several studies [18,19]. The volume of effusion can also be arbitrarily classified as: (1) minimal, if the echofree space is seen within the costophrenic angle; (2) small, if the space is over the costophrenic angle but still within a one-probe range; (3) moderate, if the space is greater than a one-probe range but

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within a two-probe range; and (4) large or massive, if the space is bigger than a two-probe range [7]. Although transthoracic US is very powerful in the evaluation of pleural effusion, differentiation of minimal effusion from organized effusion or pleural thickening may sometimes be difficult. Both lesions can appear anechoic on grayscale US, and thus, “free of echoes” is not a reliable sign for fluid collection. It has been reported that nearly 20% of echofree pleural lesions do not yield free fluid, whereas a significant percentage of complex-appearing lesions do [20]. Therefore, accurately predicting whether an echo-free or complex-appearing lesion is amenable to thoracentesis is not always possible with grayscale US. Marks et al suggested that if a pleural lesion changes its shape with respiratory excursion and if it contains movable strands or echo densities, the lesion contains fluid and can be aspirated [21]. However, these criteria still have limitations, as some loculated or small effusions do not change shape with respiration or have movable septa or echo densities, but are still amenable to aspiration. Another useful sign to distinguish effusion from a solid pleural lesion is the so-called “fluid color sign” of pleural effusion [22,23]. It was observed that true fluid, even in cases of loculated or small effusions, may generate a color flow pattern during the respiratory or cardiac cycle and thus display a turbulent color signal with color Doppler imaging (Fig. 5). In a study

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Fig. 5. Fluid color sign to differentiate minimal effusion from a solid pleural lesion. (A) True fluid generates a color flow pattern during respiratory or cardiac cycles on color Doppler ultrasound. (B) Organized pleural thickening or pleural tumor appears as a colorless pleural lesion on color Doppler ultrasound.

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Transthoracic Ultrasound comprising 76 patients, relatively high sensitivity (89.2%) and specificity (100%) of the fluid color sign in recognizing minimal fluid collection have been demonstrated [23].

(Fig. 7). Sometimes, differentiation between pleural fibrosis and pleural tumors is difficult, while USguided needle biopsy is helpful for pathologic diagnosis [26].

Pleural thickening and pleural tumors

Pneumothorax and hydropneumothorax

Pleural thickening on US is defined as echogenic lesions arising from the visceral or parietal pleurae that are greater than 3 mm in width. Pleural thickening and adhesion are usually caused by putrid pleuritis, empyema, hemothorax or iatrogenic pleurodesis. The echogenicity of the thickened pleura is variable. In putrid pleuritis resulting in pleural thickening, increasing echogenicity and septation of the pleural lesion may be seen with time as the pleural effusion becomes organized and solid, sometimes with highly echogenic shadows indicative of calcification (Fig. 6). On US, pleural tumors are well defined, hypoechoic or echogenic, solid nodular lesions located in the parietal or visceral pleurae. Primary neoplasms of the pleura are rare, except for benign and malignant mesothelioma. Metastatic pleural tumors or mesothelioma can appear as polypoid pleural nodules or sheet-like pleural thickening, usually combined with pleural effusion [16,24,25]

Transthoracic US can be helpful in the diagnosis or exclusion of clinically suspected pneumothorax [9]. US may be especially useful in urgent conditions in which no roentgenographic equipment is readily available. An important sonographic sign suggestive of pneumothorax is the loss of breathdependent lung sliding on real-time US, secondary to the accumulation of free air within the pleural cavity [10]. Broadening of the pleural line to a band can be seen occasionally. Reverberation artifacts may be markedly enhanced in small pneumothorax, but the artifacts are occasionally absent when the pneumothorax becomes more extensive [9]. In contrast, the presence of lung sliding or comet-tail artifacts excludes pneumothorax [10,11]. In patients with hydropneumothorax, the recognition of pneumothorax is easier by identifying the air–fluid level. On real-time US, loss of lung sliding above the air–fluid boundary can be verified. The downward movement of the air–fluid level during inspiration

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Fig. 6. Putrid pleuritis resulting in pleural thickening in an 82-year-old man with acute thoracic empyema. (A) On admission, ultrasound showed massive pleural effusion with sonographic septation. Closed tube drainage and intrapleural fibrinolytic therapy were performed for the empyema. PE = pleural effusion; (B) One month later, obvious thickening and adhesion of the pleura were revealed on ultrasound, with highly echogenic shadows indicative of calcification. P = pleura. J Med Ultrasound 2008 • Vol 16 • No 1

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Fig. 7. Various ultrasound images of metastatic pleural tumors. (A) Pleural nodule. (B) Polypoid pleural tumors. (C) Sheet-like pleural thickening (arrows). L = collapsed lung; PE = pleural effusion; T = pleural tumor.

impairment of lung sliding may be misinterpreted as pneumothorax by inexperienced operators. Moreover, transthoracic US is of limited use in patients with subcutaneous emphysema.

Peridiaphragmatic lesions

Fig. 8. Ultrasound image of hydropneumothorax. Note the air– fluid level (arrow). Loss of gliding sign is demonstrated above the air–fluid level on real-time ultrasound, which implies pneumothorax. During inspiration, the reverberation echoes of the pneumothorax progressively descend and present the lowering of a “curtain” that gradually masks the effusion (curtain sign). E = effusion; L = collapsed lung; PNEUMO = pneumothorax.

generates the so-called “curtain sign”, which allows the confident diagnosis of hydropneumothorax [27] (Fig. 8). It is recommended that the US findings suggestive of pneumothorax be compared with those of the healthy side of the chest. It should be noted that the gliding sign of the pleurae on real-time US comes from the movements of the pleurae during respiratory excursion. Certain conditions, such as bullae or emphysema, may result in impaired lung expansion, and subsequently, the absence or

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Radiographic elevation of a hemidiaphragm and peridiaphragmatic lesions usually pose a diagnostic problem for physicians. Using liver and spleen as a US window, US is very useful in the simultaneous evaluation of abnormalities in supradiaphragmatic, diaphragmatic and infradiaphragmatic compartments. Transthoracic US can identify basal pulmonary tumors, subphrenic abscesses, and hepatic or splenic masses located in peridiaphragmatic areas. By defining the position of the hemidiaphragm, differentiation of subpulmonary effusion and subphrenic fluid collection is relatively easy (Fig. 9). Also, the real-time visualization of diaphragm motion during respiration allows discrimination between diaphragm palsy and eventration [28].

Peripheral lung tumors On US, peripheral lung tumors appear as welldefined, homogeneous, hypoechoic or echogenic nodules with posterior acoustic enhancement. The echogenicity of the tumor increases with tumor size. Central necrosis can be detected in some

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Fig. 9. A 46-year-old man with subphrenic abscess complicated after a radical nephrectomy for left renal cell carcinoma. Chest radiograph shows elevation of left hemidiaphragm with costophrenic angle blunting (not shown). (A) Computed tomography scan reveals subphrenic abscess and left pleural effusion. (B) Ultrasound can simultaneously show pleural effusion, subphrenic abscess fluid collection, and outline of the diaphragm. A = subphrenic abscess; PE = pleural effusion; D = diaphragm. cases of large cavitary tumor. If the tumor extends to the pleura, the pleural line may be interrupted [1,3,4]. In patients with lung cancer, detection of tumor extension to the pleura and chest wall is important and may influence the subsequent treatment plan. High-resolution real-time US, particularly with higher frequency (i.e. 7.5- or 10-MHz) scanning probes, has the advantage of clear discrimination of the various soft tissue layers within the chest wall, and thus can be very valuable for determining the extent of pleural and chest wall invasion in patients with lung cancer [29]. Sugama et al [30] have defined the US criteria for the extent of tumor invasion. Ultrasound pattern (UP)1 indicates that the tumor is in contact with the visceral pleura, while UP2 means that the tumor has extended beyond the visceral pleura and is in contact with the parietal pleura, and UP3 means that the tumor has extended to the chest wall through both visceral and parietal pleurae. On US, the visceral pleura line is intact in UP1, but is invaded or interrupted in UP2 and UP3. Direct visualization of chest wall extension by the tumor can be observed in UP3. The movement of the tumor with respiration is unaltered in UP1, disturbed in UP2, and is not present in UP3 [30] (Fig. 10). In summary, disruption of the pleura, extension through the chest wall, and fixation of the tumor during breathing

on US are indicators of pleural and chest wall involvement [29,30]. Pulmonary arteriovenous malformations are frequently located in the periphery of lungs and may, therefore, be detected with transthoracic US. Pulmonary arteriovenous malformations on US appear as well-defined hypoechoic nodules, with turbulent blood flow through the lesion on color Doppler imaging. Flow signals into and out of the lesion, as well as their anatomic continuity, can be clearly demonstrated. The characteristic of low-impedance flow can be shown by spectral wave analysis (Fig. 11). US can also reveal a decrease or disappearance of flow in these lesions after effective arterial embolization [31].

Pulmonary consolidation, lung abscess, and obstructive pneumonitis The consolidated lung on US may appear as a wedge-shaped hypoechoic lesion that can move with respiration. The margin is typically irregular or serrated. The air bronchogram within the consolidation may present as bifurcating hyperechoic lines arising from the hilar region. These hyperechoic air densities can move with respiration on real-time US (Fig. 12A). Microabscesses in necrotizing pneumonia can be detected as scattered hypoechoic to anechoic spaces within the irregular-shaped J Med Ultrasound 2008 • Vol 16 • No 1

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Fig. 10. Ultrasound patterns (UP) of tumor invasion to the pleura and chest wall. (A) UP1 indicates that the tumor is in contact with the visceral pleura. The visceral and parietal pleurae lines are intact, and smooth respiratory movement of the tumor is visible on real-time ultrasound. (B) UP2 indicates the tumor extends beyond the visceral pleura, and is in contact with the parietal pleura. The visceral pleura line is thus interrupted, and the respiratory movement of the tumor is disturbed on real-time ultrasound. (C) UP3 indicates the tumor extends to the chest wall through the visceral and parietal pleurae. There is no respiratory movement of the tumor. Note that the invaded ribs are seen as hyperechoic plate-like shadows inside the lesion (arrows). (D) Computed tomography scan from the same patient as in Figure (C). PAE = posterior acoustic enhancement; Pp = parietal pleura; Pv = visceral pleura; T = tumor. consolidation. Some of the microabscesses may have hyperechoic speckled densities which represent air echoes inside the cavity [32]. In the case of a lung abscess, the air within the cavity may appear as a hyperechoic area with a posterior acoustic shadow (Fig. 12B). The air–fluid level of the cavity can be demonstrated if the patient is scanned in the sitting position. The hyperechoic air portion is depicted in the upper part of the lesion, whereas the dependent fluid portion is inhomogeneous and echogenic [33] (Fig. 12C). Transthoracic US can be useful in differentiating between a lung abscess and empyema. The ultrasonographic characteristics of a lung abscess include

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an irregular wall width, a blurred outer margin, an oval or round shape, an acute chest wall angle, and a negative pleural separation [34]. ”Fluid bronchogram” is a very useful sign indicative of bronchial obstruction, and the presence of this sign in an appropriate clinical context should raise suspicion of obstructive pneumonitis. On US, fluid bronchogram is identified as branching hyperechoic tubular structures with an anechoic interior lumen, representing the dilated fluid-filled airways within the consolidation (Fig. 13). Fluid bronchogram usually parallels the pulmonary vessels, but shows no blood flow signals on color Doppler US [35,36]. In cases of tumor causing obstructive

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Fig. 11. Pulmonary arteriovenous malformation. (A) Computed tomography scan shows a well-defined, enhanced mass in the left upper lung. (B) On grayscale ultrasound (US), the lesion appears as a well-defined, homogenous and hypoechoic mass with posterior acoustic enhancement. (C, D) Color Doppler US and amplitude US angiography indicate a tangled vascular structure with clear vessel outline and anatomic continuity. Also note the low impedance flow characteristics on spectral wave analysis. M = mass.

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Fig. 12. (A) Ultrasound (US) image of pulmonary consolidation as a wedge-shaped hypoechoic lesion with bifurcating hyperechoic lines arising from the hilum. The hyperechoic lines are air densities within the airways of the consolidated lung (air bronchogram). These hyperechoic lines can move with respiration on real-time US. Localized pleural effusion is also noted. (B) US image of lung abscess. The air portion is depicted as a hyperechoic area casting a characteristic acoustic shadow below the lesion (arrowheads). (C) US image of infected bullae in a 41-year-old man. US clearly shows the air–fluid level (arrow) while the patient is scanned in the sitting position. The air portion is depicted in the upper part of the lesion, whereas the dependent fluid portion is inhomogeneous, with echogenic densities within the abscess fluid. PE = pleural effusion; A = air portion; F = abscess fluid. J Med Ultrasound 2008 • Vol 16 • No 1

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Fig. 13. Ultrasound image of fluid bronchogram as branching hyperechoic tubular structures with an anechoic interior lumen. Fluid bronchogram usually parallels the pulmonary vessels, but shows no blood flow signals on color Doppler ultrasound. pneumonitis, the obstructing tumor can usually be shown as a well-defined, homogeneous or heterogeneous, hypoechoic nodule inside the consolidation, generally located near the hilum [35,36]. Color Doppler US can facilitate the detection of blood flow signals of the regional pulmonary vessels within a consolidated lung [8,37]. The pulmonary vessels appear as colored, branching tubular or curvilinear signals extending from the hilum to the periphery of the consolidation. The color flow signals in the pulmonary artery are usually directed toward the scanning probe, while the pulmonary venous flow signals are usually in parallel with the pulmonary artery signals with different colors, indicating the reverse direction of flow. Before attempting TNB of a consolidation, vascular structures should be verified on color Doppler US so that the puncture route can be selected to avoid injury to the vessels. There are several other applications of color Doppler imaging in the evaluation of pulmonary consolidations [8,37]. Firstly, the displacement of consistent flow signals to one side of the consolidation is a useful sign to signify a space occupying lesion (tumor or abscess) within the consolidation. Secondly, color Doppler imaging can be helpful in distinguishing pulmonary infarction from other pulmonary opacities. In pulmonary infarction, because of the occlusion of the

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pulmonary artery by thromboemboli, US may show a consolidation with no or few pulmonary artery signals. This characteristic sonographic finding is termed “consolidation with little perfusion”. Following treatment, the reperfusion of a pulmonary infarction can also be assessed with color Doppler US [38]. Color Doppler US has also been described as an adjunct method in the diagnosis of pulmonary sequestration, a congenital maldevelopment resulting in nonfunctioning lung tissue. The characteristic color Doppler US findings in pulmonary sequestration include: (1) a large tortuous pulsating feeding artery in the consolidated lung; (2) spectral wave analysis showing this vessel to be a systemic feeding artery with a pulsating artery waveform; and (3) color Doppler mapping delineating that the blood flow originates from the descending aorta [39].

Mediastinal masses Mediastinal tumors in contact with the chest wall can be assessed through a parasternal approach [40]. A suprasternal or supraclavicular approach through the paratracheal soft tissue space can be used to detect tumors located in the upper mediastinum, usually with the patient lying supine and neck extended [41]. Mediastinal lesions, such as thymic tumors, lymphomas, dermoid cysts, germ cell tumors and aneurysms of great vessels, can be shown using these approaches. On US, cysts have thin walls and anechoic contents. Most thymomas are well defined and hypoechoic, and the capsule can be well demonstrated. In patients with invasive thymoma, disruption of the capsule or invasion to the heart or pericardium can be identified with US. Lymphomas or germ cell tumors may exhibit cystic change and heterogeneous echogenicity (Fig. 14). Evaluation of a mediastinal lesion using US, particularly in conjunction with color Doppler US, has the advantage of good discrimination between the great vessels and the target mass. Therefore, the hazard of puncturing great vessels in the mediastinum during US-guided mediastinal biopsy can be avoided [40,41].

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C Sternum Lung AsA Tumor Fig. 14. A 28-year-old woman with anterior mediastinal tumor. (A, B) Chest radiography and computed tomography scan show a mass in the anterior mediastinum. (C) Ultrasound through the parasternal approach discloses a hypoechoic heterogenous tumor adjacent to the ascending aorta. Histologic diagnosis of malignant lymphoma was made by ultrasound-guided transthoracic needle biopsy. AsA = ascending aorta.

US-guided Interventional Procedures and their Uses in the Diagnosis and Management of Chest Diseases Transthoracic US can guide various invasive or interventional procedures including diagnostic thoracentesis, closed tube drainage for pleural effusion, and TNB. US guidance increases the success rate and decreases the complications associated with these procedures. The lesions can be accurately visualized and localized with US before the procedure is performed, especially when the lesion is small. More importantly, transthoracic US can provide real-time images during these procedures. A puncture transducer can be used to perform US-guided TNB with real-time visualization of the puncture route and the lesion, which enables the operator to ascertain exactly what the needle is targeting or has punctured. When a vascular

lesion is highly suspected or a lesion is close to great vessels, color Doppler imaging or amplitude US angiography can be used to identify blood flow signals within or surrounding the lesion, thus avoiding accidental puncture to vascular structures during the procedure [1,3–7]. The main contraindication to these procedures is hemorrhagic diathesis. However, mild coagulation abnormalities are acceptable for simple thoracentesis. Other contraindications include uncooperative patients who are unable to control breathing or cough on demand, especially when the lesion is small. The site of aspiration or biopsy should exclude the presence of local cutaneous lesions such as pyoderma. Although the risk of complications decreases with US guidance, these procedures should still be performed with caution in patients with borderline respiratory failure or severe emphysema [1,3,4,7]. J Med Ultrasound 2008 • Vol 16 • No 1

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US-guided thoracentesis and closed tube drainage for pleural effusion For pleural effusion of unknown etiology, it is usually necessary to obtain the fluid for cytologic, biochemical or microbiologic examination. Transthoracic US is superior to chest radiography in identifying fluid collection and choosing the optimal site for diagnostic thoracentesis [4,42]. The largest and most accessible area of fluid accumulation can be identified, and the depth for needle penetration can be measured by US. US-guided thoracentesis is particularly useful when the effusion is minimal or loculated, when tedious radiographic study is not possible, or when safe thoracentesis is mandatory in a critically ill patient [2,43]. With real-time US, direct visualization of the effusion during thoracentesis is even applicable. These US-guided measures help to improve the success rate of thoracentesis and avoid complications such as pneumothorax [4]. By differentiating minimal or loculated effusion from pleural thickening using the US criteria described earlier, US helps to predict the presence of fluid in the pleural space and to decide whether it is amenable to thoracentesis. In brief, a pleural space, which changes shape with respiration or contains movable stands or echo densities on grayscale US, or displays a fluid color sign on color Doppler US, indicates the presence of fluid accumulation and is amenable to thoracentesis [21–23]. There are several clinical situations in which closed tube drainage for effusion is needed. These include huge effusions compromising the respiratory condition, complicated parapneumonic effusion and empyema, hemothorax, and malignant effusion preparing for pleurodesis. Complications related to these drainage procedures, such as laceration of the lung, diaphragm, liver and spleen, could be disastrous. Malposition of the tube can result in failure of drainage, particularly in loculated effusion. As with diagnostic thoracentesis, it is clear that transthoracic US can decrease the risk of malposition and other complications by identifying a suitable site for the procedure [44]. On a few occasions, the liver or spleen has been mistaken for a fluid collection on US. Thus, it would be wise for inexperienced operators

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to identify the diaphragm and upper abdominal organs before puncture, to ensure that the target pleural lesion is indeed above the diaphragm [45].

US-guided needle biopsy of the pleura There are some advantages in using transthoracic US in guiding needle biopsy of pleural lesions. One advantage of US-guided pleural biopsy is related to possible focal pleural involvement in various diseases. Because focal pleural thickening or pleural tumors can be clearly identified with US, biopsy can be aimed at the local area with sonographic abnormalities. The chances of obtaining pleural tissues with significant pathologic findings will thus increase. Another advantage of real-time US is that the advance of the needle can be monitored, and over-penetration of the needle into the underlying lung parenchyma can be prevented. This is particularly true for patients with minimal pleural effusion or even without pleural effusion [4,26].

US-guided TNB for histologic diagnosis of thoracic lesions Transthoracic US can be used to guide TNB of the chest wall, peripheral pulmonary lesions or mediastinal lesions, for either fine-needle aspiration for cytologic and microbiologic analyses or large-bore needle biopsy for histologic diagnosis [1,3–5,46–48]. The choice of fine-needle aspiration or large-bore biopsy depends greatly on local pathologic expertise and is too complex to discuss in detail in this article. In general, fine-needle aspiration for cytologic examination may be sufficient for clinical management in cases of primary lung cancer. However, concerns arise regarding the reliability of nonspecific, benign or negative results. Although multiple passes may improve the diagnostic yield for malignant lesions, a negative result for fine-needle aspiration does not confidently exclude malignancy. It should be noted that an adequate histologic specimen is generally required for benign lesions, mediastinal masses, and some malignancies, such as lymphomas and sarcomas [46–48]. In a comparative study, it was demonstrated that transthoracic large-bore Tru-Cut biopsy under US guidance

Transthoracic Ultrasound

A

B

Collapsed lung

Heart

Fig. 15. Ultrasound (US) guidance improves diagnostic yield of TNB for malignant tumors with necrosis. (A) Computed tomography scan shows a large lung mass with extensive central necrosis and left pleural effusion in a 60-year-old woman. (B) US clearly reveals the necrotic center (*) and solid portion of the tumor (arrows). The histologic diagnosis of spindle cell sarcoma was made by transthoracic needle biopsy of the mural portion of tumor under US guidance. can be as safe as US-guided fine-needle aspiration, and that the diagnostic accuracy is significantly higher than that of fine-needle aspiration [47]. In our institution, we almost routinely perform fine-needle aspiration first with a 20–22-gauge needle containing an outer sheath and inner stylet. The aspiration materials placed onto glass slides are divided into two groups: one group is air-dried and the other is fixed in 95% alcohol. Papanicolaou stain is used on the alcohol-fixed slides, while Liu stain and Gram stain are used on the air-dried slides. Liu stain, which is completed in only 3 minutes, can be performed at the bedside and used for immediate microscopic examination to assess the adequacy of the specimens. If the specimens are judged inadequate or inconclusive, or if histologic specimens are required, large-core cutting biopsies are then performed with a 16-, 18- or 20-gauge Tru-Cut needle for conventional histologic examinations. Patients referred for US-guided TNB should be carefully assessed for the location, sonographic pattern, and blood flow information of the lesion by grayscale and color Doppler US. Attention should be focused on the lesion that is most likely to be accessible using a percutaneous approach. Once it has been determined that a lesion is amenable to TNB, care is taken to ensure the puncture

route and depth (usually assisted with a precise puncture transducer), to avoid penetrating the aerated lung, great vessels or major bronchi. During TNB, the tip of the needle and, occasionally, the needle shaft can be seen as an echogenic focus on the real-time US monitor, thus allowing advance of the needle to the target lesion with precision. Small peripheral lung nodules may move considerably with respiration and are often obscured by overlying ribs. These factors may make TNB difficult. However, with real-time US monitoring, TNB can be performed in a specific phase of respiration that renders the nodule most accessible and evident. Successful localization and biopsy of tumors as small as 1 cm have been possible using this approach [49,50]. TNB for large lung masses is generally not difficult. However, large lung masses frequently have extensive areas of central necrosis, so that only a small part of the tumor remains viable. Aspiration or biopsy of the central necrotic portion of a malignant tumor may yield a false negative result. US guidance can improve the diagnostic yield of TNB in such cases by delineating the solid portion of the tumor and directing sampling of these mural regions [51] (Fig. 15). For patients with Pancoast or superior sulcus tumors, although US evaluation is often handicapped by interference from the scapulae and ribs, satisfactory demonstration J Med Ultrasound 2008 • Vol 16 • No 1

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T.H. Tsai, J.S. Jerng, P.C. Yang of the lesion is often achieved by the supraclavicular approach. US is helpful in assessing the local extent of tumor involvement and guiding the needle directly to the apical lung tumor for histologic diagnosis. Because great vessels may be present in the surrounding area in such cases, color Doppler US can be used to provide detailed vascular information prior to TNB [52]. A lung tumor lacking pleural contact but with an accessible US window can also be sampled under US guidance. For patients with lung tumors associated with obstructive pneumonitis, fiberoptic bronchoscopy is usually the standard diagnostic approach. However, if the obstructing lesion is extraluminal, fiberoptic bronchoscopy may reveal only external compression and satisfactory diagnostic material cannot be obtained with either bronchoscopic biopsy or transbronchial needle aspiration. These patients may be subjected to USguided TNB to establish the histologic diagnosis of the obstructing tumor [35,36]. Using the consolidated lung as a US window, US can clearly delineate the central tumor and adjacent consolidated lung. Although some obstructing tumors are deep-seated and located near the hilum, it is usually possible to obtain sufficient specimens for cytologic or histologic diagnosis. The route of the puncture needle can be selected to avoid major bronchi and pulmonary vessels of the consolidated lung under real-time US guidance, and thus, the complication of major bleeding can be minimized. Accurate histologic diagnosis of a mediastinal mass is a cornerstone for planning appropriate treatment. Surgery is curative for thymoma, teratoma, and neurogenic tumor, but is not indicative for lymphoma, and should not be performed for metastatic lesions from pulmonary or extrapulmonary sites. Transthoracic US evaluation of mediastinal masses followed by a US-guided biopsy is a rapid and safe method of obtaining specimens for histologic examinations. Transthoracic US has the advantage of good discrimination between great vessels and the target mass, particularly in conjunction with color Doppler US. The biopsy of mediastinal tumors under real-time US guidance avoids

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accidental puncture of great vessels and vital structures in the mediastinum [40,41]. Because the diagnostic accuracy using fine-needle aspiration is lower in lymphoma, thymic tumors, and benign lesions, large-bore needle biopsy is generally recommended for mediastinal lesions [40,48].

US-guided fine-needle aspiration for microbiologic diagnosis of pulmonary infections Transthoracic US can be useful in evaluating focal pulmonary infiltrates and guiding fine-needle aspiration for microbiologic diagnosis of pulmonary infections [1,3,4,32]. Use of this invasive technique may enable accurate microbiologic diagnosis of unusual pulmonary infections, which is especially helpful in immunocompromised patients [53]. In pulmonary consolidations, the fluid-containing air spaces become a good US window, and lesions deep-seated in the consolidated lung can be visualized with transthoracic US. Parapneumonic effusion, abscess formation or tumor with obstructive pneumonitis can be clearly demonstrated. Thoracentesis of empyema or parapneumonic effusion can be performed safely under the guidance of US, even if the fluid collection is localized and minimal. Transthoracic fine-needle aspiration under US guidance provides reliable and non-contaminated specimens for microbiologic stain and culture. In patients with necrotizing pneumonia, US can be used as a guide in the needle aspiration of microabscesses [4,32]. For lung abscesses in the lung periphery, high-resolution real-time US can identify the areas where the visceral pleura adheres to the parietal pleura (lesionpleura symphysis), thus preventing pneumothorax and spillage of abscess material into the pleural cavity during needle aspiration. US can also provide precise guidance of the needle tip to the fluid portion of the abscess and ensure aspiration of an adequate amount of fluid for bacterial culture. The results of cultures obtained from US-guided abscess aspiration have been found to be superior to those obtained from sputum, blood, and bronchoalveolar lavage fluid [33]. A similar technique can be applied for drainage of abscess fluid if it is clinically indicated.

Transthoracic Ultrasound Pulmonary cryptococcosis is not a rare disease in both immunocompetent and immunocompromised hosts, and possesses the potential for dissemination. A definite diagnosis of pulmonary cryptococcosis requires a specific histopathologic examination and a positive culture. Serum cryptococcal antigen is often negative in such cases. Therefore, a timely and correct diagnosis of pulmonary cryptococcosis is often difficult. Because the lesions of pulmonary cryptococcosis tend to be subpleural in location, specimens can usually be obtained with US-guided needle aspiration for fungal isolation. Cryptococci can also be directly detected after the lung aspirates have been stained with Liu or Papanicolaou stain or with India ink [54]. In addition, direct determination of crytoptococcal antigen in lung aspirates has been shown to be a rapid and useful method for diagnosis of pulmonary cryptococcosis, and can be more reliable than isolation of this organism [55]. US-guided transthoracic fine-needle aspiration through the consolidated lung is relatively safe. US helps to select an area where the consolidation is complete and where there is no air-containing tissue interposed between the lesion and pleura. The major bronchi and vessels within the consolidation can be clearly identified by high-resolution US in conjugation with color Doppler US. The route for needle aspiration can be selected to avoid these vital structures, and thus, the complications of major bleeding and pneumothorax can be minimized [4,32]. It should be noted that the etiology of pulmonary consolidation is diverse. Although infectious pneumonia is the most common, noninfectious diseases such as lymphoma and bronchioloalveolar cell carcinoma may also present as pulmonary consolidations. US-guided large-bore biopsy has been proved useful and relatively safe for histologic diagnosis of pulmonary consolidation of unknown etiology [32].

Conclusion Advances in transducer design, signal processing, and Doppler technology have greatly improved the imaging quality of US. By scanning through the US

window, transthoracic US is a very reliable and informative imaging modality for evaluating lesions of the chest wall, pleural cavity, perdiaphragmatic area, mediastinum, and peripheral lung. The range of chest diseases for which transthoracic US may yield diagnostic information has greatly expanded. Color Doppler US further increases the diagnostic potential and safety of invasive procedures. US guidance increases the success rate while decreasing the complications of many interventional procedures such as thoracentesis, closed tube drainage for pleural effusion, and needle biopsy of the pleura. With real-time US monitoring and precise punctureguiding devices, US can be used effectively to guide TNB and other invasive procedures in the thorax. Although US-guided TNB requires certain expertise, the technique is relatively easy to master and can be performed in many situations where computed tomography-guided aspiration or biopsy would previously have been used. Our experience with transthoracic US suggests that it considerably enhances the diagnostic and therapeutic capabilities of chest physicians, improves patient care, is efficient and cost-effective, and has become an indispensable imaging tool in modern chest medicine.

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